High throughput screening for compounds that alter muscle cell glycosylation identifies new role for N-glycans in regulating sarcolemmal protein abundance and laminin binding

Journal of Biological Chemistry

Volumn 287, Issue 27, 2012, Pages 22759-22770

  Cabrera, Paula V ^a   Pang, Mabel ^a   Marshall, Jamie L ^b   Kung, Raymond ^a   Nelson, Stanley F ^a   Stalnaker, Stephanie H ^c   Wells, Lance ^c   Crosbie Watson, Rachelle H ^b   Baum, Linda G ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN CYTOSKELETON; C2C12 CELLS; CELL SURFACES; CYTOPLASMIC DOMAINS; CYTOSKELETAL PROTEINS; DYSTROPHIN; EXTRACELLULAR MATRICES; GENETIC MODIFICATIONS; GLYCANS; HIGH THROUGHPUT SCREENING; LAMININ; MUSCLE CELL; MUSCULAR DYSTROPHY; N-GLYCAN PROCESSING; N-GLYCANS; SKELETAL MUSCLE CELLS; TRANSMEMBRANE GLYCOPROTEINS; UTROPHIN; WILD TYPES;

CELL MEMBRANES; ESTERIFICATION; GENETIC ENGINEERING; GLYCOPROTEINS; MAMMALS; PROTEINS;

GLYCOSYLATION;

ALPHA DYSTROGLYCAN; AMINO ACID; CELL MEMBRANE PROTEIN; ERGOCALCIFEROL; FELBINAC; GLYCAN; LAMININ; LIOTHYRONINE; LOBELINE; N ACETYLLEUCINE; NORGESTREL; UNCLASSIFIED DRUG; UTROPHIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURFACE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG IDENTIFICATION; DRUG MECHANISM; GLYCOSYLATION; HIGH THROUGHPUT SCREENING; IN VITRO STUDY; MALE; MOUSE; MUSCLE CELL; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROCESSING; SARCOLEMMA; WILD TYPE;

ANIMALS; CELLS, CULTURED; GLYCOMICS; GLYCOSYLATION; LAMININ; LOBELINE; MALE; MANNOSYLTRANSFERASES; MICE; MICE, INBRED MDX; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCULAR DYSTROPHY, DUCHENNE; MYOBLASTS, SKELETAL; NICOTINIC AGONISTS; PLANT LECTINS; POLYSACCHARIDES; QUADRICEPS MUSCLE; RECEPTORS, N-ACETYLGLUCOSAMINE; RNA, SMALL INTERFERING; SARCOLEMMA;

MUS; WISTERIA FLORIBUNDA;

EID: 84863303578     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.334581     Document Type: Article

References (39)

1. Michele, D. E., and Campbell, K. P. (2003) Dystrophin-glycoprotein complex. Post-translational processing and dystroglycan function. J. Biol. Chem. 278, 15457-15460 (Pubitemid 36799650)
2. Ervasti, J. M. (2007) Dystrophin, its interactions with other proteins, and implications for muscular dystrophy. Biochim. Biophys. Acta 1772, 108-117
3. Blake, D. J., Tinsley, J. M., and Davies, K. E. (1994) The emerging family of dystrophin-related proteins. Trends Cell Biol. 4, 19-23 (Pubitemid 24038743)
4. Ohlendieck, K., Ervasti, J. M., Matsumura, K., Kahl, S. D., Leveille, C. J., and Campbell, K. P. (1991) Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron 7, 499-508
5. Tinsley, J., Deconinck, N., Fisher, R., Kahn, D., Phelps, S., Gillis, J. M., and Davies, K. (1998) Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat. Med. 4, 1441-1444 (Pubitemid 28553471)
6. Nguyen, H. H., Jayasinha, V., Xia, B., Hoyte, K., and Martin, P. T. (2002) Overexpression of the cytotoxic T cell GalNAc transferase in skeletal muscle inhibits muscular dystrophy in mdx mice. Proc. Natl. Acad. Sci. U.S.A. 99, 5616-5621 (Pubitemid 34411598)
7. Jayasinha, V., Hoyte, K., Xia, B., and Martin, P. T. (2003) Overexpression of the CT GalNAc transferase inhibits muscular dystrophy in a cleavage-resistant dystroglycan mutant mouse. Biochem. Biophys. Res. Commun. 302, 831-836 (Pubitemid 36294049)
8. Xu, R., Chandrasekharan, K., Yoon, J. H., Camboni, M., and Martin, P. T. (2007) Overexpression of the cytotoxic T cell (CT) carbohydrate inhibits muscular dystrophy in the dyW mouse model of congenital muscular dystrophy 1A. Am. J. Pathol. 171, 181-199 (Pubitemid 47339238)
9. Xu, R., DeVries, S., Camboni, M., and Martin, P. T. (2009) Overexpression of Galgt2 reduces dystrophic pathology in the skeletal muscles of α-sarcoglycan-deficient mice. Am. J. Pathol. 175, 235-247
10. Yoon, J. H., Chandrasekharan, K., Xu, R., Glass, M., Singhal, N., and Martin, P. T. (2009) The synaptic CT carbohydrate modulates binding and expression of extracellular matrix proteins in skeletal muscle. Partial dependence on utrophin. Mol. Cell Neurosci. 41, 448-463
11. Bozzi, M., Morlacchi, S., Bigotti, M. G., Sciandra, F., and Brancaccio, A. (2009) Functional diversity of dystroglycan. Matrix Biol. 28, 179-187
12. Yoshida-Moriguchi, T., Yu, L., Stalnaker, S. H., Davis, S., Kunz, S., Madson, M., Oldstone, M. B., Schachter, H., Wells, L., and Campbell, K. P. (2010) O-Mannosyl phosphorylation of α-dystroglycan is required for laminin binding. Science 327, 88-92
13. Stalnaker, S. H., Hashmi, S., Lim, J. M., Aoki, K., Porterfield, M., Gutierrez-Sanchez, G., Wheeler, J., Ervasti, J. M., Bergmann, C., Tiemeyer, M., and Wells, L. (2010) Site mapping and characterization of O-glycan structures on α-dystroglycan isolated from rabbit skeletal muscle. J. Biol. Chem. 285, 24882-24891
14. Hara, Y., Kanagawa, M., Kunz, S., Yoshida-Moriguchi, T., Satz, J. S., Kobayashi, Y. M., Zhu, Z., Burden, S. J., Oldstone, M. B., and Campbell, K. P. (2011) Like-acetylglucosaminyltransferase (LARGE)-dependent modification of dystroglycan at Thr-317/319 is required for laminin binding and arenavirus infection. Proc. Natl. Acad. Sci. U.S.A. 108, 17426-17431
15. Sgambato, A., and Brancaccio, A. (2005) The dystroglycan complex. From biology to cancer. J. Cell Physiol. 205, 163-169
16. Esapa, C. T., Bentham, G. R., Schröder, J. E., Kröger, S., and Blake, D. J. (2003) The effects of post-translational processing on dystroglycan synthesis and trafficking. FEBS Lett. 555, 209-216 (Pubitemid 37486031)
17. Kawahara, G., Karpf, J. A., Myers, J. A., Alexander, M. S., Guyon, J. R., and Kunkel, L. M. (2011) Drug screening in a zebrafish model of Duchenne muscular dystrophy. Proc. Natl. Acad. Sci. U.S.A. 108, 5331-5336
18. Rooney, J. E., Welser, J. V., Dechert, M. A., Flintoff-Dye, N. L., Kaufman, S. J., and Burkin, D. J. (2006) Severe muscular dystrophy in mice that lack dystrophin and α7 integrin. J. Cell Sci. 119, 2185-2195 (Pubitemid 43960308)
19. Peter, A. K., Ko, C. Y., Kim, M. H., Hsu, N., Ouchi, N., Rhie, S., Izumiya, Y., Zeng, L., Walsh, K., and Crosbie, R. H. (2009) Myogenic Akt signaling up-regulates the utrophin-glycoprotein complex and promotes sarcolemma stability in muscular dystrophy. Hum. Mol. Genet 18, 318-327
20. Kimura, E., Han, J. J., Li, S., Fall, B., Ra, J., Haraguchi, M., Tapscott, S. J., and Chamberlain, J. S. (2008) Cell-lineage regulated myogenesis for dystrophin replacement. A novel therapeutic approach for treatment of muscular dystrophy. Hum. Mol. Genet 17, 2507-2517
21. Yang, Y. H., Dudoit, S., Luu, P., Lin, D. M., Peng, V., Ngai, J., and Speed, T. P. (2002) Normalization for cDNA microarray data. A robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30, e15
22. Aoki, K., Perlman, M., Lim, J. M., Cantu, R., Wells, L., and Tiemeyer, M. (2007) Dynamic developmental elaboration of N-linked glycan complexity in the Drosophila melanogaster embryo. J. Biol. Chem. 282, 9127-9142 (Pubitemid 47093502)
23. Orlando, R., Lim, J. M., Atwood, J. A., 3rd, Angel, P. M., Fang, M., Aoki, K., Alvarez-Manilla, G., Moremen, K. W., York, W. S., Tiemeyer, M., Pierce, M., Dalton, S., and Wells, L. (2009) IDAWG. Metabolic incorporation of stable isotope labels for quantitative glycomics of cultured cells. J. Proteome Res. 8, 3816-3823
24. Ceroni, A., Maass, K., Geyer, H., Geyer, R., Dell, A., and Haslam, S. M. (2008) GlycoWorkbench. A tool for the computer-assisted annotation of mass spectra of glycans. J. Proteome Res. 7, 1650-1659
25. Gundry, R. L., Raginski, K., Tarasova, Y., Tchernyshyov, I., Bausch-Fluck, D., Elliott, S. T., Boheler, K. R., Van Eyk, J. E., and Wollscheid, B. (2009) The mouse C2C12 myoblast cell surface N-linked glycoproteome. Identification, glycosite occupancy, and membrane orientation. Mol. Cell Proteomics 8, 2555-2569
26. Xia, B., Hoyte, K., Kammesheidt, A., Deerinck, T., Ellisman, M., and Martin, P. T. (2002) Overexpression of the CT GalNAc transferase in skeletal muscle alters myofiber growth, neuromuscular structure, and laminin expression. Dev. Biol. 242, 58-73 (Pubitemid 34113670)
27. Barresi, R., Michele, D. E., Kanagawa, M., Harper, H. A., Dovico, S. A., Satz, J. S., Moore, S. A., Zhang, W., Schachter, H., Dumanski, J. P., Cohn, R. D., Nishino, I., and Campbell, K. P. (2004) LARGE can functionally bypass α-dystroglycan glycosylation defects in distinct congenital muscular dystrophies. Nat. Med. 10, 696-703 (Pubitemid 38937634)
28. Patnaik, S. K., and Stanley, P. (2005) Mouse large can modify complex Nand mucinO-glycans on α-dystroglycan to induce laminin binding. J. Biol. Chem. 280, 20851-20859 (Pubitemid 40776790)
29. Zhang, Z., Zhang, P., and Hu, H. (2011) LARGE expression augments the glycosylation of glycoproteins in addition to α-dystroglycan conferring laminin binding. PLoS One 6, e19080
30. Sántha, E., Sperlágh, B., Zelles, T., Zsilla, G., Tóth, P. T., Lendvai, B., Baranyi, M., and Vizi, E. S. (2000) Multiple cellular mechanisms mediate the effect of lobeline on the release of norepinephrine. J. Pharmacol. Exp. Ther. 294, 302-307 (Pubitemid 30434701)
31. Dwoskin, L. P., and Crooks, P. A. (2002) A novel mechanism of action and potential use for lobeline as a treatment for psychostimulant abuse. Biochem. Pharmacol. 63, 89-98 (Pubitemid 34158807)
32. Wilhelm, C. J., Johnson, R. A., Eshleman, A. J., and Janowsky, A. (2008) Lobeline effects on tonic and methamphetamine-induced dopamine release. Biochem. Pharmacol. 75, 1411-1415
33. Lee, W. C., Kang, D., Causevic, E., Herdt, A. R., Eckman, E. A., and Eckman, C. B. (2010) Molecular characterization of mutations that cause globoid cell leukodystrophy and pharmacological rescue using small molecule chemical chaperones. J. Neurosci. 30, 5489-5497
34. Kanagawa, M., Saito, F., Kunz, S., Yoshida-Moriguchi, T., Barresi, R., Kobayashi, Y. M., Muschler, J., Dumanski, J. P., Michele, D. E., Oldstone, M. B., and Campbell, K. P. (2004) Molecular recognition by LARGE is essential for expression of functional dystroglycan. Cell 117, 953-964 (Pubitemid 38798860)
35. Zhang, P., and Hu, H. (2012) Differential glycosylation of α-dystroglycan and proteins other than α-dystroglycan by like-glycosyltransferase. Glycobiology 22, 235-247
36. Hu, Y., Li, Z. F., Wu, X., and Lu, Q. (2011) Large induces functional glycans in an O-mannosylation dependent manner and targets GlcNAc terminals on α-dystroglycan. PLoS One 6, e16866
37. Aguilan, J. T., Sundaram, S., Nieves, E., and Stanley, P. (2009) Mutational and functional analysis of Large in a novel CHO glycosylation mutant. Glycobiology 19, 971-986
38. Lefeber, D. J., Schönberger, J., Morava, E., Guillard, M., Huyben, K. M., Verrijp, K., Grafakou, O., Evangeliou, A., Preijers, F. W., Manta, P., Yildiz, J., Grünewald, S., Spilioti, M., van den Elzen, C., Klein, D., Hess, D., Ashida, H., Hofsteenge, J., Maeda, Y., van den Heuvel, L., Lammens, M., Lehle, L., and Wevers, R. A. (2009) Deficiency of Dol-P-Man synthase subunit DPM3 bridges the congenital disorders of glycosylation with the dystroglycanopathies. Am. J. Hum. Genet. 85, 76-86
39. Capaldi, M. J., Dunn, M. J., Sewry, C. A., and Dubowitz, V. (1985) Lectin binding in human skeletal muscle. A comparison of 15 different lectins. Histochem. J. 17, 81-92 (Pubitemid 15144436)